How do recent changes in Lake Erie affect birds? Part three: type-E botulism - Birds Canada
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
How do recent changes in With permission of Ontario Birds Lake Erie affect birds? Part three: type-E botulism Doug Tozer and Gregor Beck THE HEALTH OF LAKE ERIE reached a actions that we, as birders, can take to low point in the 1960s and 1970s, and help alleviate the issues. then improved greatly by the 1980s Botulism is a disease that infects (Makarewicz and Bertram 1991). Now, humans as well as wildlife (Critchley Lake Erie is suffering from harmful algal 1991). It is caused by neurotoxins pro- blooms, botulism, invasive species, cli- duced by the bacterium Clostridium bot- mate change and other issues. Why is ulinum (Desta et al. 2016). There are sev- this? What has brought about so many eral types or strains of C.botulinum (types new issues? What does it all mean for A through H), each surviving best under birds? This review article is the last of a different conditions (Hannett et al. series of three articles in Ontario Birds. 2011). Botulism rarely infects humans The articles provide an overview of some because thorough cooking, good hygiene of the current environmental and eco- and other routine measures prevent the logical issues for Lake Erie, with empha- acquisition of the toxins (Shapiro et al. sis on the implications for the numerous 1998). A few of the strains infect wild bird species that depend on the lake for birds: type-C causes die-offs of waterfowl nesting and migration. There are dozens throughout the world, particularly in of worthy issues to profile. We chose to western North America (Wobeser et al. begin, in part one, with invasive Phrag- 1987) and type-E causes die-offs in the mites (Tozer and Beck 2018); in part two, Great Lakes (Wijesinghe et al. 2015). C. we tackled invasive Zebra Mussels and botulinum is a native species that occurs Quagga Mussels (Dreissena polymorpha in soils and sediments throughout the and D. rostriformis bugensis, respectively; Great Lakes (Graikoski et al. 1968). It Tozer and Beck 2019); and here, in part survives for long periods, sometimes for three, we take on the impacts of type-E many decades, as harmless dormant botulism. In addition to a review of each spores, but once favourable growing con- issue, the articles present new analysis of ditions are encountered it starts growing relevant citizen science data and suggest and produces botulinum neurotoxin 84 Ontario Birds August 2019
Figure 1. Tens of thousands of individuals belonging to dozens of different waterbird species, such as this
Common Loon, sometimes die during late summer and autumn on Lake Erie and the other Great Lakes
due to outbreaks of type-E botulism. Photo: Bird Studies Canada
(Long and Trauscher 2006). The neuro- benefit to the bacteria (Poulain and
toxin is one of the most potent toxins Popoff 2019). As such, survival is just as
known (Singh 2000) and although many high and distribution in the environment
aspects of the disease have been well- is just as extensive in toxic and non-toxic
studied for nearly two centuries (Cher- forms of certain strains of C. botulinum
ington 2004), the function that the toxin (Poulain and Popoff 2019). Therefore,
serves for the bacteria, if there is one, the current type-E botulism issue for
remains unclear (Simpson 1986). Alter- waterbirds (i.e., any aquatic bird species)
natively, the toxin may be a by-product in Lake Erie and the rest of the Great
of a complicated evolutionary history Lakes might ultimately be attributable to
involving lateral transfer of toxin-pro- a mere chance event deep in C. botu-
ducing genes to the bacteria, perhaps linum’s evolutionary history!
from a virus, with no obvious subsequent
Volume 37 Number 2 85
The problem for waterbirds, or any found dead, whereas in 2002, one of the
other vertebrate such as fish, is that worst years on record, over 20,000 indi-
botulinum toxin interferes with trans- viduals washed up dead on beaches and
mission of nerve impulses intended to shorelines throughout the Great Lakes
stimulate peripheral or voluntary muscles (Cabrera 2014). The number of dead
(Desta et al. 2016). Through a series of individuals recorded is, of course, only an
different steps, the toxin prevents the unknown fraction of the total number
neurotransmitter acetylcholine from killed, given that carcasses sink before
traveling out from nerve endings, effec- they wash up on shore or carcasses wash
tively killing nerve impulses so they never up in locations where they go unrecord-
reach intended muscles (Gundersen ed. Recent research using radio transmit-
1980). The result is flaccid paralysis, and ters implanted in floating Common
waterbirds with even very small doses of Loon carcasses released throughout Lake
the toxin are unable to keep their eyes Michigan aimed to uncover how wind,
open, raise their wings, move their feet, waves and water currents influence the
or hold up their heads, hence the com- trajectory of floating carcasses, which will
mon name “limberneck disease” (Cher- help identify botulism hotspots and may
ington 2004). In the end, infected water- help better understand how many car-
birds typically die a slow death due to casses go undetected (Kenow et al. 2016).
starvation, drowning, depredation, or What happened starting in the late
other complications (Figure 1). 1990s and early 2000s to cause annual
The occurrence and magnitude of die-offs of waterbirds in Lake Erie and
waterbird mortalities due to type-E bot- most of the other Great Lakes? The quick
ulism is highly variable over space and answer is: we don’t really know. Evidence
time (Lafrancois et al. 2011). Die-offs of is building to suggest that recurring type-
waterbirds were first recorded in the E botulism is the result of multiple, com-
Great Lakes in the early 1960s, contin- plicated, interacting pathways of infec-
ued sporadically during the 1970s and tion involving nutrient runoff, invasive
1980s and were absent during most of species, algal blooms, climate change and
the 1990s (Brand et al. 1983, 1988; Cab- perhaps additional factors yet to be dis-
rera 2014). Die-offs of waterbirds due to covered. The basics go like this: C. botu-
type-E botulism have occurred annually linum spores become activated and pro-
in Lake Huron since 1998, Lake Erie duce toxin when they encounter warm
since 1999 and Lake Ontario since 2002 water with abundant nutrients and no
(Cabrera 2014). The die-offs involve a oxygen (Espelund and Klaveness 2014).
variety of different species including We know from long-term monitoring
loons, grebes, herons, cormorants, ducks, that water temperature (Mason et al.
coots, shorebirds, eagles, gulls, terns and 2016), extent of deoxygenated water or
crows (Carpentier 2000, Canadian hypoxia (Zhou et al. 2013) and soluble
Cooperative Wildlife Health Centre reactive phosphorus (Daloğlu et al.
2008, Chipault et al. 2015). In some 2012) have all increased in recent decades
years, only a small number of birds are in Lake Erie and some of the other
86 Ontario Birds August 2019
Great Lakes. The result: increasingly good season, which is more likely to wash
conditions for production of botulism downstream into the lakes during increas-
neurotoxin. ingly frequent storms, themselves a con-
Now add a dash of invasive species and sequence of climate change (Smith et al.
a pinch of algae. C. botulinum spores 2015). Indeed, the overall enhancing
become very active and produce large effect of the mussels on algal growth has
amounts of neurotoxin within hot, oxy- been shown convincingly through exper-
gen-depleted, nutrient-rich mats of rot- imental manipulation using pre-con-
ting algae of the genus Cladophora (most- structed “colonies” of live and dead mus-
ly C. glomerata, hereafter “Cladophora”), sels either with or without artificial addi-
which piles up in shallow water and along tion of nutrients (Francoeur et al. 2017).
shorelines in late summer (Byappanahalli In short, bring in non-native invasive
and Whitman 2009, Chun et al. 2013, mussels, clear the water column, increase
2015). Submerged aquatic vegetation the light, increase the nutrients, bring on
dominated by Cladophora has increased in the Cladophora and produce lots of bot-
extent in all of the Great Lakes in recent ulism neurotoxin in dead mats of algae
decades as shown by remote sensing satel- at the end of the summer. As further
lite data (Brooks et al. 2015). The increase evidence of these relationships, multiple
in Cladophora is in part due to increases studies show correlations at various scales
in water clarity and associated light pene- between type-E botulism outbreaks in
tration brought about by the super-effi- waterbirds and warm water, low water
cient filter feeding of non-native invasive (shallow water tends to be warmer) and
Zebra Mussels and Quagga Mussels, Cladophora (Wijesinghe et al. 2015, Princé
which remove light-blocking phytoplank- et al. 2017).
ton and other particles from the water How do botulism bacteria or its neu-
column (Auer et al. 2010). The increase rotoxin get from rotting mats of algae or
in Cladophora is also due to increases in other sources into waterbirds? One way is
hard substrate for Cladophora to attach to through invertebrates such as fly maggots
in the form of the mussels’ shells, since (Diptera larva) that pick up the bacteria
Cladophora only grows on hard surfaces or toxin while feeding on or within rot-
and not on soft mud or sand (Higgins et ting carcases or algae washed up along the
al. 2008). The mussels also concentrate lakeshore. Notably, invertebrates such as
nutrients for Cladophora by filtering aquatic insects and mussels are unaffected
nutrients out of the water column and by the neurotoxin (Pérez-Fuentetaja et al.
eliminating them in their feces (Hecky 2011). Shorebirds feed on the tainted
et al. 2004, Dayton et al. 2014). The invertebrates (Figure 2) and gulls and
enhancement of algal growth by the mus- other scavengers feed on the infected car-
sels is made even stronger by recent cases, and in turn can become infected.
increases in nutrient runoff into Lake Erie These pathways are likely the most com-
and the other Great Lakes due to increas- mon in the summer and early fall (Cana-
es in surface application of fertilizer on dian Cooperative Wildlife Health Centre
agricultural fields during the non-growing 2008). The presence of botulism bacteria
Volume 37 Number 2 87
Figure 2. Some waterbirds, such as this Spotted Sandpiper, become infected with type-E botulism bacteria or its toxin while feeding on or within tainted algae washed up along lakeshores. Photo: Leslie Abram or its toxin is also found at high levels in the tissues of living and dead Zebra Mus- sels and Quagga Mussels, as well as in various other aquatic invertebrates, such as larval midges (Chironomidae) and worms (Oligochaeta) (Pérez-Fuentetaja et al. 2006, 2011). The chironomids, oligochetes and other non-mussel inver- tebrates likely acquire the bacteria or its toxin through direct ingestion or while eating detritus or sediment, particularly near rotting algae, whereas the mussels likely acquire the toxin by filtering it out of the water column or filtering out specializes in feeding on non-native inva- smaller invertebrates that have already sive mussels and is itself especially com- acquired it (Getchell and Bowser 2006, mon in the stomachs of botulism-killed Pérez-Fuentetaja et al. 2006). Certain waterbirds, particularly cormorants and waterfowl, such as the Long-tailed Duck loons (Hebert et al. 2014, Essian et al. (Clangula hyemalis), Common Golden- 2016, King et al. 2017). Furthermore, eye (Bucephala clangula) and Bufflehead botulism-infected fish that are partially (B. albeola) feed on the tainted mussels paralyzed are attractive, easy pickings for and the toxin-laden aquatic invertebrates fish-eating waterbirds (Yule et al. 2006). (Schummer et al. 2008a,b). Fish feed The pathways leading up through aquat- on the infected mussels and other infect- ic invertebrates, mussels and fish to ed invertebrates and due to biomagnifi- waterbirds are likely the most common cation acquire high concentrations of in autumn (Canadian Cooperative the bacteria or toxin (Bott et al. 1966). Wildlife Health Centre 2008). There are The tainted fish are in turn fed on by a probably other sources and production variety of different waterbirds (Essian et pathways of botulism yet to be discov- al. 2016). In an ironic final twist, anoth- ered or better described, such as water er non-native invasive species, the currents that bring spores up from the Round Goby (Neogobius melanostomus), sediment so they are available to enter 88 Ontario Birds August 2019
the food chain and additional complicat- for answering this type of timely but
ing factors involving competition unforeseen question. As shown above,
between C. botulinum and other micro- there are dozens of waterbird species that
organisms that keep botulism bacteria at are potentially affected by type-E botu-
low numbers (Pérez-Fuentetaja et al. lism on the Great Lakes. Based on obser-
2006). The bottom line is that recurring ved mortalities, the majority of dead
outbreaks of type-E botulism on the individuals are loons, mergansers, cor-
Great Lakes over the past two decades morants and gulls (Carpentier 2000,
appear to be the result of multiple, com- Canadian Cooperative Wildlife Health
plicated, interacting ecological and envi- Centre 2008, Chipault et al. 2015). Pop-
ronmental changes ultimately brought ulations of most of these more-common-
about by non-native invasive Zebra Mus- ly killed species have remained steady or
sels and Quagga Mussels, nutrient load- increased over the past two decades in
ing and climate change. Ontario or the Great Lakes when type-E
The botulism issue is complicated botulism has been most prevalent. For
and potentially quite big, but is it actual- example, abundance of breeding Com-
ly negatively affecting waterbird popula- mon Loons was stable in Ontario during
tions? Long-term bird population moni- the period (Smith et al. 2019); abun-
toring programs are extremely important dance increased for Common Merganser
Volume 37 Number 2 89
Figure 3. Type-E botulism may be reducing the reproductive success of the Common Loon (an adult with two chicks is shown here). Photo: Missy Mandel (Mergus merganser) in southern Ontario and for Red-breasted Merganser (Mergus serrator) in northeastern North America (Canadian Wildlife Service Waterfowl Committee 2017); the number of breed- ing Double-crested Cormorants (Pha- lacrocorax auritus) increased and stabi- lized throughout the Great Lakes (Weseloh et al. 2002, Ridgway et al. 2006). Exceptions to that trend are the number of breeding gulls. Ring-billed Gulls (Larus delawarensis) and Herring Gulls (L. argentatus) declined slightly in The above examples tell us whether the Great Lakes, although this is thought abundance of infected waterbird species to be due to reduced food availability is negatively influenced by type-E botu- rather than botulism (Weseloh 2011). By lism, but they do not tell us about poten- contrast, the Great Black-backed Gull tial negative effects on reproductive suc- (L. marinus) is apparently especially cess, which could happen without con- susceptible to type-E botulism and as a current changes in population size. For result has been extirpated as a breeder example, we could see stable or nearly from eastern Lake Ontario (Shutt et al. stable populations at the same time as 2014) and may soon be eliminated as a declining reproductive success if enough breeder from throughout the Great Lakes immigrants move in from outside to (Weseloh 2011). Therefore, it seems that maintain the population. The Common the widespread die-offs caused by type-E Loon (Figure 3) seems to be especially botulism are not creating long-term vulnerable to type-E botulism given that population-level impacts—in most cases. it figures prominently in counts of botu- However, continued research and moni- lism-killed carcases that wash up on shore toring are needed to fully understand (Carpentier 2000, Canadian Cooperative population-level impacts. Wildlife Health Centre 2008, Chipault 90 Ontario Birds August 2019
et al. 2015). As such, we used data from colour-marked Common Loons, we
Bird Studies Canada’s Canadian Lakes know that reproductive success is lower
Loon Survey (Tozer et al. 2013b) to for male Common Loons breeding on a
explore the possibility that reproductive territory for the first time; apparently it
success of this hard-hit species might be takes up to two or more years for them to
negatively affected by type-E botulism. learn, by trial and error, where the best
Our line of reasoning was as follows: The nest sites are located on a territory in
Common Loon is a long-lived species (up order to maximize their reproductive suc-
to 20-30 years in the wild) and breeds cess (Piper et al. 2008). Remarkably, nest
throughout central and northern On- sites in this species are chosen by males,
tario, well to the north of the lower Great regardless of previous nesting experience
Lakes where botulism outbreaks are most of females, for reasons that remain
common (Evers 2007). Individuals typi- unclear (Piper et al. 2008). We also know
cally spend the first few years of their lives from colour-marked individuals that the
on the ocean and at 3-4 years of age number of young produced per year for
return to the breeding grounds for the males but not females increases with
first time to acquire a breeding territory increasing age up to 15-17 years old
(Piper et al. 2015). Based on studies of (Piper et al. 2017). If enough breeding
Volume 37 Number 2 91
males die due to botulism on their south- We explored these ideas using data
ward migration through the lower Great from 11,623 Common Loon breeding
Lakes each autumn, then as a result, we attempts on 1,317 lakes spread across 38
would expect a larger proportion of years in Ontario (Figure 4). Following
younger, inexperienced, first-time territo- Tozer et al. (2013a), we modeled the
rial males in the breeding population the number of six-week-old young per terri-
following spring and thereafter, with an torial pair per year from 1981 to 2018
associated reduction in reproductive suc- while controlling statistically for lake size
cess over the years. Thus, if type-E botu- and longitude given that the number of
lism negatively affects the reproductive young produced is known to increase
success of Common Loons, we would with increasing lake size (Alvo 2009,
expect higher chick production, on aver- Piper et al. 2012) and is higher in the west
age, before the onset of recurring type-E compared to the east (Tozer et al. 2013a).
botulism outbreaks in the late 1990s and We also included a random effect for each
early 2000s and lower chick production lake because ~50% of the lakes surveyed
after that time. each year, on average, had reproductive
Figure 4. Lakes with at least one year of data collected by participants in Bird Studies Canada’s Canadian
Lakes Loon Survey used to determine patterns in Common Loon reproductive success in Ontario between
1981 and 2018 (n = 1,317 lakes).
ONTARIO
Survey lake
92 Ontario Birds August 2019Botulism rare
1.00
Botulism throughout lower
Great Lakes in most years
Six-week-old young/pair/year
0.75
0.50
1981 1986 1991 1996 2001 2006 2010 2016
success data for > 1 pair of loons (Tozer Figure 5. Reproductive success of Common
et al. 2013a). We focused on six-week-old Loons in Ontario between 1981 and 2018.
young because Common Loons of this Shown are annual estimates (dots) and
age have attained nearly adult size and associated 95% confidence intervals (vertical
gray lines). A loess line of best fit (curved blue
with it a much lower chance of being
line) is included to show overall trajectory.
depredated, making them a reasonable The orange horizontal dashed line denotes an
indicator of the number of young actual- estimate of the minimum number of young per
ly fledged (Evers 2007). Even though pair per year (0.48) required to prevent popula-
acidity is a strong predictor of loon repro- tion declines (Evers 2007). Years of extremely
ductive success (Alvo et al. 1988, Alvo good chick production (i.e., at or above 0.75
2009), we were unable to control for dif- young per pair per year) ceased to occur after
ferences in pH due to lack of data. We 1999 when recurring type-E botulism spread
found the number of young per pair per throughout the lower Great Lakes.
Data source: Bird Studies Canada’s
year was highly variable, with no clear
Canadian Lakes Loon Survey
difference in reproductive success before
and after the onset of recurring type-E
botulism in the late 1990s and early
2000s (Figure 5). Nonetheless, it is worth
noting that years of extremely good chick
production (i.e., at or above 0.75 young
Volume 37 Number 2 93So what does it all mean? We have
seen that type-E botulism in waterbirds
in Lake Erie and the lower Great Lakes is
due to multiple, complicated, interacting
ecological and environmental changes
ultimately brought about by non-native
invasive species, nutrient loading, climate
change and probably other factors. There-
fore, we cannot stress enough to be
extremely careful regarding these issues,
especially taking steps to avoid introduc-
ing and spreading non-native invasive
species (see summary at Ministry of Nat-
ural Resources and Forestry 2019), a con-
cluding message we also arrived at in each
of our first two articles in this three-part
Botulism-killed Common Loon. series (Tozer and Beck 2018, 2019). Any-
Photo: Bird Studies Canada thing we can do to reduce nutrient load-
ing and climate change in the Great Lakes
per pair per year) ceased to occur after will also help mitigate the type-E botu-
1999 when recurring type-E botulism lism issue for waterbirds (see Environ-
started to spread throughout the lower mental Commissioner of Ontario 2018
Great Lakes (Figure 5). a,b). In particular, there are actions we
Whether this pattern is linked to bot- can all take as individuals to help mitigate
ulism is unknown. Of course, there are climate change (see Environmental Com-
many other factors that influence repro- missioner of Ontario 2019). In the end,
ductive success of Common Loons, perhaps the most important action we
including acid precipitation, mercury can collectively take as birders to help
pollution and climate change, any com- alleviate botulism and the many other
bination of which might also explain the issues currently affecting Lake Erie and
pattern, but the influence of botulism is the lower Great Lakes is to inform every-
worth considering. On a happy note, the one that there is much more at stake than
number of Common Loon chicks pro- most people typically appreciate. All too
duced in most of the years since the early often, the negative effects that these issues
2000s is apparently high enough to main- have on humans receive the most atten-
tain a stable population given the average tion by the media and the general public,
number of young per pair per year in whereas the negative implications for
most years is above 0.48 (Figure 5), which waterbirds tend to go unnoticed or unad-
is the best available estimate of the mini- dressed. This is where we, as birders, can
mum number required to prevent popu- help in a big way to achieve a healthier
lation declines (Evers 2007). balance.
94 Ontario Birds August 2019Acknowledgements Brand, C.J., S.M. Schmitt, R.M. Duncan
In this review, we use information col- and T.M. Cooley. 1988. An outbreak of type
lected by hundreds of Bird Studies Cana- E botulism among common loons (Gavia
da’s citizen scientists, an impressive num- immer) in Michigan’s Upper Peninsula.
Journal of Wildlife Diseases 24:471-476.
ber of whom are Ontario Field Ornithol-
ogists members (thank you!). Support to Brooks, C., A. Grimm, R. Shuchman, M.
the authors while preparing this article Sayers and N. Jessee. 2015. A satellite-based
multi-temporal assessment of the extent of
has been provided by the John and Pat
nuisance Cladophora and related submerged
McCutcheon Charitable Foundation. We aquatic vegetation for the Laurentian Great
thank members of the Scientific Advisory Lakes. Remote Sensing of Environment
Committee of Bird Studies Canada’s 157:58-71.
Long Point Waterfowl and Wetlands Byappanahalli, M.N. and R.L. Whitman.
Research Program for comments that 2009. Clostridium botulinum type E occurs
improved the paper. and grows in the alga Cladophora glomerata.
Canadian Journal of Fisheries and Aquatic
Sciences 66:879-882.
Literature Cited
Cabrera, S. 2014. Botulism outbreaks.
Alvo, R. 2009. Common Loon, Gavia immer, Pp. 99-110 In State of the Great Lakes 2011.
breeding success in relation to lake pH and Cat No. En161-3/1-2011E-PDF. EPA 950-R-
lake size over 25 years. Canadian Field- 13-002. Available: https://binational.net//wp-
Naturalist 123:146–156. content/uploads/2014/11/sogl-2011-techni-
Alvo, R., D.J.T. Hussell and M. Berrill. cal-report-en.pdf (Accessed: 11 June 2019).
1988. The breeding success of common loons Canadian Cooperative Wildlife Health
(Gavia immer) in relation to alkalinity and Centre. 2008. Type E Botulism in Canada.
other lake characteristics in Ontario. Unpublished manuscript. University of
Canadian Journal of Zoology 66:746-752. Guelph, Guelph, Ontario.
Auer M.T., L.M. Tomlinson, S.N. Higgins, Canadian Wildlife Service Waterfowl
S.Y. Malkin, E.T. Howell and H.A. Boots- Committee. 2017. Population Status of
ma. 2010. Great Lakes Cladophora in the Migratory Game Birds in Canada: November
21st century: same algae—different ecosys- 2017. CWS Migratory Birds Regulatory
tem. Journal of Great Lakes Research Report Number 49, Gatineau, Québec.
36:248-255. Available: https://www.canada.ca/en/environ
Bott, T.L., J.S. Deffner, E. McCoy and ment-climate-change/services/migratory-
E.M. Foster. 1966. Clostridium botulinum game-bird-hunting/consultation-process-
type E in fish from the Great Lakes. Journal regulations/report-series/population-status-
of Bacteriology 91:919-924. 2017.html (Accessed: 11 June 2019).
Brand, C.J., R.M. Duncan, S.P. Garrow, Carpentier, G. 2000. Avian botulism
D. Olson and L.E. Schumann. 1983. outbreak along the lower Great Lakes.
Waterbird mortality from botulism type E in Ontario Birds 18:84-91.
Lake Michigan: an update. Wilson Bulletin Cherington, M. 2004. Botulism: update and
95:269-275. review. Seminars in Neurology 24:155-162.
Volume 37 Number 2 95Chipault, J.G., C.L.White, D.S. Blehert, Environmental Commissioner of Ontario.
S.K. Jennings and S.M. Strom. 2015. Avian 2018b. Climate action in Ontario: what’s next?
botulism type E in waterbirds of Lake Michi- 2018 greenhouse gas progress report. Toronto,
gan, 2010–2013. Journal of Great Lakes Ontario. Available: https://docs.assets.eco.on.
Research 41:659-664. ca/reports/climate-change/2018/Climate-
Chun, C.L., C.I. Kahn, A.J. Borchert, Action-in-Ontario.pdf (Accessed: 11 June
M.N. Byappanahalli, R.L.Whitman, J. Peller, 2019).
C. Pier, G. Lind, E.A. Johnson and M.J. Environmental Commissioner of Ontario.
Sadowsky. 2015. Prevalence of toxin-produc- 2019. Climate pollution: reducing my foot-
ing Clostridium botulinum associated with the print backgrounder. Toronto, Ontario. Avail-
macroalga Cladophora in three Great Lakes: able: http://docs.assets.eco.on.ca/reports/other
growth and management. Science of the Total publications/Reducing-My-Footprint.pdf
Environment 511:523-529. (Accessed: 11 June 2019).
Chun, C.L., U. Ochsner, M.N. Byappana- Espelund, M. and D. Klaveness. 2014.
halli, R.L. Whitman, W.H. Tepp, G. Lin, Botulism outbreaks in natural environments—
E.A. Johnson, J. Peller and M.J. Sadowsky. an update. Frontiers in Microbiology 5:article
2013. Association of toxin-producing Clostrid- 287. doi:10.3389/fmicb.2014.00287.
ium botulinum with the macroalga Cladophora
Essian, D.A., J.G. Chipault, B.M. Lafrancois
in the Great Lakes. Environmental Science
and J.B.K. Leonarda. 2016. Gut content
and Technology 47:2587-2594.
analysis of Lake Michigan waterbirds in years
Critchley, E.M.R. 1991. A comparison of with avian botulism type E mortality, 2010-
human and animal botulism: a review. Journal 2012. Journal of Great Lakes Research
of the Royal Society of Medicine 84:295-298. 42:1118-1128.
Daloğlu, I., K.H. Cho and D. Scavia. 2012. Evers, D.C. 2007. Status assessment and
Evaluating causes of trends in long-term dis- conservation plan for the Common Loon
solved reactive phosphorus loads to Lake Erie. (Gavia immer) in North America. BRI Report
Environmental Science and Technology 2007-20. U.S. Fish and Wildlife Service,
46:10660-10666. Hadley, MA. Available: http://www.briloon.
Dayton, A.I., M.T. Auer and J.F. Atkinson. org/uploads/BRI_Documents/Loon_Center/
2014. Cladophora, mass transport, and the RCF/USFWS_Conservation_Plan_92913-
nearshore phosphorus shunt. Journal of Great 1.pdf (Accessed: 11 June 2019).
Lakes Research 40:790-799.
Francoeur, S.N., K.A. Peters Winslow,
Desta, S., M. Melaku and N. Abdela. 2016. D. Miller and S.D. Peacor. 2017. Mussel-
Botulinum toxin and its biological significance: derived stimulation of benthic filamentous
a review. World Applied Sciences Journal algae: the importance of nutrients and spatial
34:854-864. scale. Journal of Great Lakes Research
Environmental Commissioner of Ontario. 43:69-79.
2018a. Agricultural runoff: excess phosphorus Getchell, R.G. and P.R. Bowser. 2006.
contributing to algal blooms, Section 2.3. Pp. Ecology of type e botulism within dreissenid
72-82 In Back to basics, 2018 Environmental mussel beds. Aquatic Invaders 17:1-8.
Protection Report, Clean water, Volume 2,
Polluting our waters, Chapter 2. Toronto,
Ontario. Available: https://docs.assets.eco.on.
ca/reports/environmental-protection/2018/
Back-to-Basics.pdf (Accessed: 11 June 2019).
96 Ontario Birds August 2019Graikoski, J.T., E.W. Bowman, R.A. King, L.E., S.R. deSolla, J.R. Marentette,
Robohm and R.A. Koch. 1968. Distribution R.A. Lavoie, T.K. Kyser, L.M. Campbell,
of Costridium botulinum in the ecosystem of M.T. Arts and J.S. Quinn. 2017. Fatty acids,
the Great Lakes. Pp. 271-277 In Herzberg, M, stable isotopes, and regurgitate reveal diet dif-
ed., Proceedings of the First U.S.-Japan Con- ferences between Lake Ontario and Lake Erie
ference on toxic micro-organisms. United double-crested cormorants (Phalacrocorax
States-Japan Cooperative Program in Natural auritus). Journal of Great Lakes Research
Resources Joint Panels on Toxic Micro-organ- 43:132-140.
isms and the U.S. Department of the Interior, Lafrancois, B.M., S.C. Riley, D.S. Blehert
Washington, D.C. Available: https://archive. and A.E. Ballmann. 2011. Links between
org/details/bub_gb_CLpTkoNVlkMC/page/ type E botulism outbreaks, lake levels, and
n2 (Accessed: 11 June 2019). surface water temperatures in Lake Michigan,
Gundersen, C.B. 1980. The effects of botu- 1963–2008. Journal of Great Lakes Research
linum toxin on the synthesis, storage and 37:86-91.
release of acetylcholine. Progress in Neuro- Long, S.C. and T. Tauscher. 2003. Watershed
biology 14:99-119. issues associated with Clostridium botulinum:
Hannett, G.E., W.B. Stone, S.W. Davis and a literature review. Journal of Water and
D. Wroblewski. 2011. Biodiversity of Health 4:277-88.
Clostridium botulinum type E associated with Makarewicz, J.C. and P. Bertram. 1991.
a large outbreak of botulism in wildlife from Evidence for the restoration of the Lake Erie
Lake Erie and Lake Ontario. Applied and ecosystem. Bioscience 41:216-223.
Environmental Microbiology 77:1061-1068.
Hebert, C.E., J. Chao, D. Crump, T.B.
Johnson, M.D.Rudy, E. Sverko, K.Williams,
D. Zaruk and M.T. Arts. 2014. Ecological
tracers track changes in bird diets and possible
routes of exposure to Type E botulism. Journal
of Great Lakes Research 40:64-70.
Hecky, R.E., R.E.H. Smith, D.R. Barton,
S.J. Guildford, W.D. Taylor, M.N. Charlton
and T. Howell. 2004. The nearshore phospho-
rus shunt: a consequence of ecosystem engin-
eering by dreissenids in the Laurentian Great
Lakes. Canadian Journal Fisheries and Aquatic
Sciences 61:1285-1293. Long Point
Higgins, S.N., S.Y. Malkin, E.T. Howell, S.J.
Guildford, L. Campbell, V. Hiriart-Baer and
Birders Cottage
R.E. Hecky. 2008. An ecological review of
331 Erie Blvd is steps away
Cladophora glomerata (Chlorophyta) in the from migration hotspots
Laurentian Great Lakes. Journal of Phycology Old Cut Bird Observatory
44:839-854. and Long Point Provincial Park
Kenow, K.P., Z. Ge, L.J. Fara, S.C. Houdek SPRING, SUMMER & FALL RENTALS
and B.R. Lubinski. 2016. Identifying the
origin of waterbird carcasses in Lake Michigan Contact Adam Timpf
using a neural network source tracking model. adam.timpf@gmail.com
Journal of Great Lakes Research 42:637-648.
Volume 37 Number 2 97Mason, L.A., C.M. Riseng, A.D. Gronewold, Poulain, B. and M.R. Popoff. 2019. Why are
E.S. Rutherford, J. Wang, A. Clites, S.D.P. botulinum neurotoxin-producing bacteria so
Smith and P.B. McIntyre. 2016. Fine-scale diverse and botulinum neurotoxins so toxic?
spatial variation in ice cover and surface Toxins 11:34.
temperature trends across the surface of the Princé, K., J.G. Chipault, C.L.White and
Laurentian Great Lakes. Climatic Change B. Zuckerberg. 2017. Environmental condi-
138:71-83. tions synchronize waterbird mortality events
Ministry of Natural Resources and Forestry. in the Great Lakes. Journal of Applied Ecology
2019. Stop the spread of invasive species. 55:1327-1338.
Queen’s Printer for Ontario. Available: Ridgway, M.S., J.B. Pollard and D.V.C.
https://www.ontario.ca/page/stop-spread-inva Weseloh. 2006. Density-dependent growth
sive-species (Accessed: 9 February 2019). of double-crested cormorant colonies on Lake
Pérez-Fuentetaja, A., M.D. Clapsadl, Huron. Canadian Journal of Zoology
D. Einhouse, P.R. Bowser, R.G. Getchell 84:1409-1420.
and W. T. Lee. 2006. Influence of Schummer, M.L., S.A. Petrie and R.C.
limnological conditions on Clostridium Bailey. 2008a. Dietary overlap of sympatric
botulinum type E presence in Eastern Lake diving ducks during winter on northeastern
Erie sediments (Great Lakes, USA). Lake Ontario. Auk 125:425-433.
Hydrobiologia 563:189-200.
Schummer, M.L., S.A. Petrie and R.C.
Pérez-Fuentetaja, A., M.D. Clapsadl, R.G. Bailey. 2008b. Interaction between macroin-
Getchell, P.R. Bowser and W. T. Lee. 2011. vertebrate abundance and habitat use by
Clostridium botulinum type E in Lake Erie: diving ducks during winter on northeastern
inter-annual differences and role of benthic Lake Ontario. Journal of Great Lakes Research
invertebrates. Journal of Great Lakes Research 34:54-71.
37:238-244.
Shapiro, R.L., C. Hatheway and D.L.
Piper, W.H., C. Walcott, J.N. Mager and Swerdlow. 1998. Botulism in the United
F.J. Spilker. 2008. Nestsite selection by male States: a clinical and epidemiologic review.
loons leads to sex-biased site familiarity. Annals of Internal Medicine 129:221-228.
Journal of Animal Ecology 77:205-210.
Shutt, J.L., D.W. Andrews, D.V.C.Weseloh,
Piper, W.H., J.N. Mager, C. Walcott, D.J. Moore, C.E. Hebert, G.D. Campbell
L. Furey, N. Banfield, A. Reinke, F. Spilker and K. Williams. 2014. The importance of
and J.A. Flory. 2015. Territory settlement in island surveys in documenting disease-related
common loons: no footholds but age and mortality and Botulism E in Great Lakes
assessment are important. Animal Behaviour colonial waterbirds. Journal of Great Lakes
104:155e163. Research 40:58-63.
Piper, W.H., J.S. Grear and M.W. Meyer. Simpson, L.L. 1986. Molecular pharmacology
2012. Juvenile survival in common loons of botulinum toxin and tetanus toxin. Annual
Gavia immer: effects of natal lake size and Review of Pharmacology and Toxicology
pH. Journal of Avian Biology 43:280-288. 26:427-53.
Piper, W.H., K.M. Brunk, J.A. Flory and Singh, B.R. 2000. Intimate details of the most
M.W. Meyer. 2017. The long shadow of poisonous poison. Nature Structural Biology
senescence: age impacts survival and territory 7:617-619.
defense in loons. Journal of Avian Biology
48:1062-1070.
98 Ontario Birds August 2019Smith, A.C., M.-A.R. Hudson, V. Aponte and Weseloh, D.V.C., C. Pekarik, T. Havelka,
C.M. Francis. 2019. North American Breed- G. Barrett and J. Reid. 2002. Population
ing Bird Survey – Canadian Trends Website, trends and colony locations of double-crested
Data-version 2017. Environment and Climate cormorants in the Canadian Great Lakes and
Change Canada, Gatineau, Quebec, K1A 0H3. immediately adjacent areas, 1990-2000:
Available: https://wildlife-species.canada.ca/ a manager’s guide. Journal of Great Lakes
breeding-bird-survey-results (Accessed: 4 July Research 28:125-144.
2019). Wijesinghe, R.U., R.J. Oster, S.K. Haack,
Smith, D.R., K.W. King and M.R. Williams. L.R. Fogarty, T.R. Tucker and S.C. Riley.
2015. What is causing the harmful algal blooms 2015. Spatial, temporal, and matrix variability
in Lake Erie? Journal of Soil and Water Conser- of Clostridium botulinum Type E toxin gene
vation 70:27A-29A. distribution at Great Lakes beaches. Applied
Tozer, D. and G. Beck. 2018. How do recent and Environmental Microbiology 81:13.
changes in Lake Erie affect birds? Part one: Wobeser, G., S. Marsden and R.J. MacFar-
invasive Phragmites. Ontario Birds 36:161-169. lane. 1987. Occurrence of toxigenic Clostri-
Tozer, D. and G. Beck. 2019. How do recent dium botulinum type C in the soil of wetlands
changes in Lake Erie affect birds? Part two: in Saskatchewan. Journal of Wildlife Diseases
Zebra Mussels and Quagga Mussels. Ontario 23:67-76.
Birds 37:29-42. Yule, A.M., I.K. Barker, J.W. Austin and
Tozer, D.C., C.M. Falconer and D.S. Bad- R.D. Moccia. 2006. Toxicity of Clostridium
zinski. 2013a. Common Loon reproductive botulinum type E neurotoxin to great lakes
success in Canada: the west is best but not for fish: implications for avian botulism. Journal
long. Avian Conservation and Ecology 8:1. of Wildlife Diseases 42:479-493.
Tozer, D.C., C.M. Falconer and D.S. Bad- Zhou, Y., D.R. Obenour, D. Scavia, T.H.
zinski. 2013b. The Canadian Lakes Loon Johengen and A.M. Michalak. 2013. Spatial
Survey 1981-2012: 32 years of monitoring and temporal trends in Lake Erie hypoxia,
Common Loons as indicators of ecosystem 1987−2007. Environmental Science and
health. Bird Studies Canada, Port Rowan, ON. Technology 47:899-905.
Available: https://www.birdscanada.org/
volunteer/clls/resources/CLLSsummary.pdf
(Accessed: 11 June 2019). Doug Tozer
Long Point Waterfowl and Wetlands
Weseloh, D.V.C. 2011. Inland colonial
Research Program
waterbird and marsh bird trends for Canada.
Bird Studies Canada
Canadian Biodiversity: Ecosystem Status and
P.O. Box 160
Trends 2010 Technical Thematic Report No.
Port Rowan, Ontario N0E 1M0
18. Canadian Councils of Resource Ministers.
E-mail: dtozer@birdscanada.org
Ottawa, ON. http://www.biodivcanada.ca/
default.asp?lang=En&n=137E1147 0 Gregor Beck
(Accessed: 11 June 2019). Bird Studies Canada
P.O. Box 160
Port Rowan, Ontario N0E 1M0
Volume 37 Number 2 99You can also read
